The Use of Classical Biological Control to Preserve Forests in North America

XVII Emerald ( planipennis Fairmaire) (Coleoptera: )

Leah S. Bauer1, Jian J. Duan2, and Juli R. Gould3

1USDA Forest Service, Northern Research Station, East Lansing, , 48823, USA

2USDA Agriculture Research Service, Beneficial Introduction Research Unit, Newark, Delaware, 19713, USA

3USDA APHIS PPQ, Center for Plant Health Science and Technology, Buzzards Bay, Massachusetts, 02542, USA

In the Palearctic region, in this are DESCRIPTION OF grouped into 36 subgenera and 34 informal species-groups based on morphological characters of adults (Chamorro et al., 2012). On this basis, A. planipennis was placed in the Agrilus planipennis Fairmaire, 1888 (type locality: ) is subgenus Uragrilus Semenov (Alexeev, 1998). However, considered the senior synonym to A. marcopoli Obenberger, more recent analyses using adult and larval characters 1930 (type locality: China), A. marcopoli ulmi Kurosawa, 1956 suggest A. planipennis be moved to the Agrilus cyaneoniger (type locality: ), and A. feretrius Obenberger, 1936 (type species-group (Jendek and Grebennikov, 2011; Volkovitsh locality: Taiwan) by Jendek (1994) in a revision of Eastern and Hawkeswood, 1990). Palearctic Agrilus species. Agrilus is the largest genus in the Buprestidae Distribution with ~2,800 described species worldwide (Bellamy, 2008). Countries in Asia where A. planipennis is reported include Adults of this genus are flashy, metallic-colored , China, , Russian Far East, Japan, Taiwan, Laos, and frequently collected using nets or traps (Fig. 1). However, (Ko, 1969; Kurosawa et al., 1956, 1985; Chinese Academy of Science, 1986; Yu, 1992; Akiyama and Ohmomo, 1997; Mühle, 2003; Wei et al., 2004; Fukutomi and Hori, 2004; Jendek and Grebennikov, 2011). In areas of northeast China, Korea, and the Russian Far East, the distribution of A. planipennis generally coincides with that of ash ( spp.) including F. chinensis Roxb., F. chinensis var. rhynchophylla, F. chinensis var. japonica, F. mandshurica Rupr., F. lanuginosa Koidz., and the introduced Nearctic species F. americana L., F. pennsylvanica Marsh., and F. velutina Torr. (Liu, Figure 1 Adult of (Agrilus planipennis) on ash leaf. Leah Bauer, USDA Forest Service, North- 1966; Hou, 1993; Chinese Academy of Science, 1986; Yu, ern Research Station, East Lansing, Michigan. 1992; Zhang et al., 1995; Liu et al., 1996; Liu et al., 2003; there is little interest in their immature stages, which must be Duan et al., 2012a). However, in Japan, Taiwan, and Laos, collected from inside trunks, branches, or woody stems. confirmation that A. planipennis is native will require more Consequently, critical information on the biology, population information on species of Agrilus that feed exclusively on dynamics, and host ranges of most Agrilus species is lacking. Fraxinus spp. (Mühle, 2003; Bray et al., 2011). In Mongolia,

189 The Use of Classical Biological Control to Preserve Forests in North America

the genus Fraxinus is unknown (Grubov, 1982), thus an America and Europe, respectively (Baranchikov, 2008; early, unconfirmed report of A. planipennis there is suspect Izhevskii et al., 2010). The expansion of EAB’s range to (Alexeev, 1979). the Western Palearctic region threatens European ash In 2002, A. planipennis was discovered in North species, including F. angustifolia Vahl., F. excelsior, and F. America after being reared from dead and dying ash trees ornus L. (Wessels-Berk and Scholte, 2008). The invasive from southeastern Michigan and nearby Ontario, Canada, population of EAB in North America only attacks (Haack et al., 2002). Due to the bright green coloration of A. Fraxinus spp. (Anulewicz et al., 2008), and several studies planipennis adults, this species was given the common name report that species of Nearctic and European ash are more of emerald ash borer (EAB) (Entsoc.org, 2012). In areas of attractive and susceptible to EAB attack than are species North America currently infested with EAB, its host range of Asian ash, which coevolved with EAB (Liu et al., 2003; and distribution (Fig. 2) coincides with that of Fraxinus). Rebek et al., 2008; Duan et al., 2012b).

Figure 2 The known distribution and quarantines of emerald ash borer in North America as of June 1, 2012.

Genetic studies of EAB from North America and Upon arrival in North America, EAB became Asia, and tree-ring analyses of ash trees in southeast established and spread throughout the Great Lakes Region, Michigan, indicate that this was introduced from due in part to the abundance of ash trees in the urban and China during the 1990s (Siegert et al., 2009; Bray et al., forested landscapes (MacFarlane and Meyer, 2005; Poland 2011). The most likely route of entry was EAB-infested and McCullough, 2006; Pugh et al., 2011), limited EAB ash lumber used for the manufacture of crates, palettes, resistance to attack among native ash (Rebek et al., 2008), and dunnage used in international shipping. Within a and release from its native natural enemies (Bauer et al., few years of its detection, EAB was determined to be 2004, 2005; Duan et al., 2009). Although EAB adults are the cause of ash mortality in other nearby states and capable of long-distance flight (Taylor et al., 2010), much provinces (Fig. 2). of the spread of EAB in North America is facilitated In 2006, EAB was found in Moscow, , where by human-assisted movement of infested ash firewood, it caused extensive mortality in urban plantings of F. nursery stock, and lumber (Cappaert et al., 2005; Poland pennsylvanica and F. excelsior L., ash species native to North and McCullough, 2006). In an effort to reduce the loss

190 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

of North American ash trees, regulatory agencies in both the and Canada imposed quarantines on the movement of ash materials and attempted eradication of EAB by removal of the ash trees around known infestations. The eradication efforts ended when it was found that EAB was distributed across much of central and northeastern areas of North America. Infestations of EAB are now known in 22 states (Colorado, Connecticut, Georgia, Illinois, Indiana, Iowa, Kansas, Kentucky, Figure 3 Emerald ash borer eggs are white (left) when freshly laid, but turn tan as they age (right). David Cappaert, Maryland, Massachusetts, Michigan, Minnesota, Missouri, Michigan State University, Bugwood.org. New Hampshire, New York, North Carolina, Ohio, Pennsylvania, Tennessee, Virginia, West Virginia, and Wisconsin) and Ontario and Quebec, Canada (Fig. 2).

Damage Type Emerald ash borer females lay their eggs (Fig. 3) singly or in small clusters between the layers of bark or in bark crevices of ash trees. Upon egg hatch, the neonates bore directly through the bark and into the tree until reaching the phloem and cambial region, where they feed (Cappaert et al., 2005). As larvae grow through four larval stages (Fig. 4), they leave behind increasingly large, frass- filled, serpentine galleries (Fig. 5). Larval feeding disrupts the transport of nutrients and water in the phloem and outer sapwood. At low EAB-larval densities, ash trees exhibit some immune response, notably the formation of callous around EAB galleries (Duan et al., 2012b). However, as larval densities increase over a period of two to five years, the phloem is consumed or sufficiently damaged to cause tree death (Figs. 6, 7) (Smith, 2006).

Extent The establishment and spread of EAB in North America has resulted in the death of tens of Figure 4 Feeding stage larvae of emerald ash borer: above, millions of ash trees in urban and forested ecosystems. second, third and 4th instars; below, full-grown 4th in- star. David Cappaert, Michigan State University, Bug- In forested ecosystem of the eastern United States, there wood.org. are an estimated 8 billion ash trees valued at $US 282.25 billion (Federal Register, 2003; Nowak et al., 2003). Until at $US 11.7 billion (Federal Register, 2003; Kovacs et recently, ash trees were one of the most commonly planted al., 2010). The long-term ecological effects of EAB in landscape trees in the urban environment because they forested and riparian ecosystems are more difficult to grow rapidly, tolerate adverse growing conditions, are easy quantify (Federal Register, 2007). According to a recent to propagate, and were considered resistant to most pests. study, EAB has killed virtually the entire ash canopy of The costs for removal and replacement of ash trees killed southeast Michigan, and despite ash seedlings and saplings by EAB to communities and smaller landholders are high; in gaps, recovery of an ash overstory is unlikely due to the e.g., the expense for ash removal and replacement in six continued EAB infestation across the landscape (Kashian infested southeastern Michigan counties was estimated and Witter, 2011). Models of EAB spread predict a rapid

XVII Emerald Ash Borer 191 The Use of Classical Biological Control to Preserve Forests in North America

Figure 5 Galleries caused by feeding emerald ash borer larvae. Left, Michigan Department of Agriculture, Bugwood.org. RIght, Edward Czerwinski, Ontario Ministry of Natural Resources, Bugwood.org.

Figure 6 Dead and dying ash in forest area due to emerald ash borer. Troy Kimoto, Canadian Food Inspection Agency, Bugwood.org.

192 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

Figure 7 Small trees with epicomic shoots due to the emerald ash borer. David Cappaert, Michigan State University, Bugwood.org. expansion of the infestation throughout North America layers of loose bark and in bark crevices. The eggs of (BenDor et al., 2006; Muirhead et al., 2006; Prasad et al., EAB are ca. 1.0 mm in diameter and amber in color when 2010; Mercader et al., 2011), and researchers are concerned mature. Neonate larvae hatch in about two weeks and that EAB threatens all native ash tree species (Gandhi and bore through the bark until reaching the phloem, where Herms, 2010). they make galleries in the outer sapwood and inner bark as they feed. In late summer and fall, mature fourth-instar Biology of Pest larvae excavate pupal chambers in the outer sapwood or EAB requires one or two years to complete its outer bark, where they spend the winter folded into a J development, depending on the climate and condition shape, also referred to as J-larvae (Duan et al., 2010). In of the host tree (Cappaert et al., 2005; Wang et al., 2010; early spring, the J-larvae shorten into prepupae before Tluczek et al., 2011). For EAB populations that complete pupation. The pupae gradually darken as they mature and development in a single year, adult emergence starts in after about four weeks mature into pharate adults. For the spring at 200 to 260 growing degree-days base 10°C EAB with a two-year life cycle, larvae that are immature (DD10), with peak emergence around 540 DD10 (Brown- when cold weather arrives in the fall simply overwinter in Rytlewski, 2004, McCullough and Siegert, 2007a). EAB their feeding gallery, complete development the following adults emerge from D-shaped exit holes and fly into the summer, spend their second winter as J-larvae, and emerge canopy where they feed on ash leaves. Mating begins about as adults in the following spring. a week later, and females start laying eggs two to three weeks later, preferring to oviposit on ash trees under stress (McCullough et al., 2009a,b; Mercader et al., 2011). EAB females place eggs in concealed areas such as between

XVII Emerald Ash Borer 193 The Use of Classical Biological Control to Preserve Forests in North America

Perhaps the most studied species is A. anxius due to ANALYSIS OF RELATED NATIVE periodic and damaging outbreaks in birch stands (Betula) INSECTS IN THE UNITED STATES across much of North America (Nash et al., 1951; Barter, 1957; Loerch and Cameron, 1983). These authors report Native Nontarget Species Related to the Pest a variety of from A. anxius, including five egg parasitoids from two families (Ablerus sp. [Aphelinidae]; In North America, the family Buprestidae has 53 genera, Avetienella sp., Ooencyrtus sp., Thysanus sp., [Encyrtidae]), of which Agrilus is the largest with 174 described species and over 15 species of larval parasitoids from four families (Fisher, 1928; Poole, 1997; Bellamy, 2008). Species of Agrilus (Atanycolus spp., Doryctes spp., floridanus Ashmead feed exclusively on woody angiosperms and are generally [= S. simillimus Ashmead], Wroughtonia ligator (Say) [all restricted to host species within a single genus or family. The ]; Phasgonophora sulcata Westwood [Chalcididae]; only native species in the genus known to feed on ash trees nr. rugglesi Rohwer [Eulophidae]; Bephratoides in North America is Gory, a small beetle agrili (Ashmead), Eurytoma sp. [both Erytomidae]; that feeds on the phloem of dead or dying ash twigs (Petrice and species of Ephialtes, Dolichomitus, Glypta, Ichneumon, et al., 2009). Other native wood-boring coleopterans that Olesicampe, Orthizema, Pimploterus [all Ichneumonidae]). feed on ash include species of , , , Egg parasitism averaged 55% in a New Brunswick study and (Buprestidae), Neoclytus (Cerambycidae), and and 7% in a similar study in Pennsylvania, whereas larval Hylesinus (Curculionidae) (Solomon, 1995). parasitism averaged 20% in both studies (Barter, 1957; Since the guilds of Agrilus spp. are less Loerch and Cameron, 1983). specific to host tree than to host niche (e.g., host size, and , the two-lined chestnut borer, is location of feeding larvae) (Taylor et al., 2012), some native another well-studied species prone to damaging outbreaks Agrilus are potentially susceptible to attack by parasitoids in drought-stressed oaks (Quercus spp.) and sometimes introduced for biological control of EAB. Although most American beech (Fagus grandifolia Ehrh.). This species was Agrilus are considerably smaller than EAB (>8.5-mm long originally a pest of the American chestnut (Castanea dentata adults), some overlap in parasitoid-host ranges is possible (Marsh.) Borkh.). Several authors have documented a guild between EAB and the larger species of Agrilus. Agrilus of larval parasitoids attacking A. bilineatus larvae that are species that fall in this category in eastern North America similar to those attacking A. anxius, including P. sulcata are A. acutipennis Mannerheim, A. anxius Gory, A. arcuatus (Chalcididae), Atanycolus spp., Doryctes spp., S. floridanus, and LeConte, A. bilineatus (Weber), A. burkei Fisher, A. difficilis W. ligator (Braconidae) (Chittenden, 1897; Chapman, 1915; Gory, A. horni Kerremans, A. granulatus (Say), A. liragus Dunbar and Stephens, 1976; Côté and Allen, 1980; Haack Barter & Brown, A. macer LeConte, A. nigricans Gory, A. and Benjamin, 1982; Cappaert and McCullough, 2009). Of politus (Say), and A. vittaticollis (Randall) (Solomon, 1995; these, P. sulcata was the most abundant, averaging 10.5% Parsons, 2008). These species may be at some risk of attack parasitism in A. bilineatus. No egg parasitoids are known. by introduced parasitoids targeted at EAB. The population dynamics of Agrilus liragus, a periodic pest of poplars (Populus spp.), was studied in New Brunswick Native Natural Enemies Affecting the Pest (Barter, 1965). Several parasitoids in the same genera were From Agrilus species of similar size and habits as EAB, reported, including unknown species of egg parasitoids in there are parasitoid species that also attack EAB, as has the genera Thysanus and Avetienella (Encyrtidae) and the been demonstrated by field studies of EAB in North larval parasitoids P. sulcata (Chalcididae) and S. floridanus, America (see references below). However, research on the Atanycolus spp., W. ligator, Doryctes spp., T. nr. rugglesi, and population dynamics of native Agrilus is generally limited Ephialtes sp. (Braconidae). Of these, P. sulcata was the most to pest species, which periodically experience outbreaks prevalent, with parasitism ranging from 2 to 20%. damaging to their host trees (Vansteenkiste et al., 2005). Interestingly, the guilds of egg and larval parasitoid Consequently, the literature on natural enemies of Agrilus from species of Agrilus are similar throughout the world species is largely drawn from a few pests, of which a diverse (Taylor et al., 2012). In North America, Agrilus egg group of hymenopteran parasitoids is known. parasitoids are mainly from the family Encyrtidae (4

194 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

genera/5 species), and the larval parasitoids are from the Braconidae (7 genera/19 species), Ichneumonidae HISTORY OF BIOLOGICAL (10 genera/11 species), a few species from Eulophidae CONTROL EFFORTS (2 genera), Eupelmidae (4 genera), Eurytomidae (2 genera), Pteromalidae (2 genera), and a single species of Area of Origin of Pest Chalcididae (Taylor et al., 2012). This indicates that the The emerald ash borer is native to Asia, including northeast parasitoids of Agrilus are more specific to host niches than China (Jilin, Liaoning, Heilongjiang, Hebei, and Shandong to host tree species. provinces), Korea, the Russian Far East, Taiwan, and Japan From field studies since EAB’s invasion in North (Chinese Academy of Science, 1986; Jendek, 1994; Jendek America, a diverse guild of Agrilus parasitoids has been and Grebennikov, 2011). observed attacking EAB larvae. However, parasitoid prevalence is generally low and no native egg parasitoids Areas Surveyed for Natural Enemies are known (Taylor et al., 2012). In Michigan, the two China In 2003, exploration for EAB natural enemies most abundant native larval parasitoids are the solitary began in China with the sampling of Asian (F. chinensis, F. ectoparasitoids in the genus Atanycolus (Braconidae) mandshurica) and North American (F. pennsylvanica, F. velutina) (several species) and the solitary endoparasitoid P. sulcata ash species for EAB in the cities of Beijing and Tianjin and (Chalcididae) (Cappaert and McCullough, 2009; Duan the provinces of Hebei, Heilongjiang, Jilin, Liaoning, and et al., 2012b). Other less less-common species reported Shandong (Liu et al., 2003; Liu et al., 2007). Evidence of past from studies done in Michigan, Ohio, and Pennsylvania EAB infestations or active infestations was found in each include Atanycolus hicoriae Shenefelt, A. simplex Cresson, city and province except Shandong. The authors also found A. nigropopyga Shenefelt, A. disputabilis (Cresson), S. that ash species native to North America and ash trees (of floridanus, S. laflammei, Spathius n. sp., Leluthia astigmata (all any species) planted in urban areas were more susceptible Braconidae); species of Dolichomitus, Orthizema, Cubocephalus to EAB attack than ash species native to China and those (Ichneumonidae); Eulmus sp.; and Balcha indica (Mani & growing in forested natural areas (Liu et al., 2003). Kaul) (Eupelmidae) (Bauer et al., 2005, 2008; Duan et al., 2009; Kula et al., 2010; Duan et al., 2012b). These Russian Far East From 2007–2011, surveys for EAB parasitic hymenopterans are presumed to be native except were conducted in and around the cities of Vladivostok, B. indica, which is an exotic parasitoid of wood-boring Khabarovsk, and on Sakhalin Island (Yurchenko et al., beetle larvae in the eastern United States from Southeast 2007; Williams et al., 2010; Duan et al., 2012a). Researchers Asia (Gibson, 2005). found that EAB in ash trees planted along city streets in Although several native or self-introduced hymenopteran Vladivostok, including green ash (F. pennsylvanica) from species parasitize EAB larvae in Michigan, the overall level North America, F. excelsior from Europe, and the endemic of parasitism is low (<4% combined parasitism) (Bauer et ash species F. mandshurica and F. chinensis var. rhynhophylla. al., 2008; Duan et al., 2009). However, even though such A report of EAB near the Korean border (Alexeev, parasitoids are generally scarce, Atanycolus cappaerti Marsh 1979) was not confirmed during a survey for EAB in and Strazanac was recently discovered at several Michigan 2004, nor was EAB among the 36 species of Agrilus field sites with parasitism ofEAB larvae ranging from 9% to listed in collections at the Siberian Zoological Museum, 71% (Cappaert and McCullough, 2009). In another Michigan Novosibirsk (Schaefer, 2005). study, the prevalence of Atanycolus spp. increased from <1% to 19%, and that of P. sulcata from <1% to 13%, in one year South Korea In north and central South Korea in (Duan et al., 2012b). The long-term impact that these native 2004 and 2005, researchers searched for EAB in forested parasitoids will have on EAB population density and ash areas containing F. chinensis var. rhynchophylla and F. health is still unknown and must be determined by further mandshurica (Williams et al., 2005, 2006). EAB is apparently monitoring. rare in South Korea as these surveys failed to find EAB until a small EAB population was discovered attacking water-stressed F. chinensis planted along a road near the

XVII Emerald Ash Borer 195 The Use of Classical Biological Control to Preserve Forests in North America

city of Daejeon in central South Korea in 2005. Another JJD, unpublished) and is the dominant parasitoid of EAB EAB population attacking F. chinensis trees damaged by larvae in northeast China (Liu et al., 2007). construction was found in 2007 in the Yangsuri, which is A third parasitoid of immature EAB, later described as about 50 km east of Seoul (Williams et al., 2010). Sclerodermus pupariae Yang and Yao (Wu et al., 2008; Wang et al., 2010; Yang et al., 2012), was discovered attacking EAB Japan EAB populations are extremely low and larvae and pupae in Tianjin. Due to its broad host range difficult to find in Japan, and EAB natural enemies were among woodborers (Tang et al., 2012), low prevalence in not found during foreign explorations in 2003 and 2004 China, and propensity of some species in this genus to sting (Schaefer, 2004, 2005). humans, S. pupariae was not considered further for use in biological control of EAB in the United States. Natural Enemies Found A solitary, parthenogenic egg parasitoid in the genus Historically, emerald ash borer was considered only Oobius (Encyrtidae) was reared from EAB eggs collected a minor, sporadic pest of native ash tree species in Asia. from F. mandshurica and F. pennsylvanica trees in Jilin province Thus, only limited literature was found in 2002, when in 2004. It was later described as Zhang & it was discovered in North America. However, in areas Huang (Fig. 10) (Zhang et al., 2005). Another population of China and Russia, plantings of North American ash of O. agrili was recently found in Liaoning province (JRG species, which are less resistant to EAB than are Asian ash and JJD, unpublished). In 2010, an undescribed species species, have caused an increase in EAB density since the of Oenycyrtus (Encyrtidae) was reared from EAB eggs 1960s (Yu, 1992; Zhang et al., 1995; Liu et al., 1996, 2003, 2007; Zhao et al., 2005; Duan et al., 2012a). In rural parks, nurseries, and urban areas, where many of these non- native ash trees are planted, researchers have discovered several hymenopteran parasitoid species attacking EAB larvae and eggs. Three species from northeast China are being introduced in the United States for biological control of EAB. A fourth species from Russia is being evaluated for future release.

China The first report of a parasitoid attacking EAB came from the provincial port city of Tianjin, southeast of Beijing, whre EAB had become a major pest of F. velutina, a North American ash species that was planted extensively Figure 8 Adult . Jennifer Ayer, Bugwood.org. in the region. A gregarious ectoparasitoid, later described as Spathius agrili Yang (Braconidae) (Fig. 8), was found parasitizing EAB larvae in these ash plantings (Xu, 2003; Liu et al., 2003; Yang et al., 2005). It was also collected from EAB larvae infesting F. pennsylvanica and F. mandshurica trees in Jilin province (Liu et al., 2003) and in Beijing (LSB, unpublished). Spathius agrili is the dominant parasitoid of EAB in Tianjin (Wang et al. 2010); however, it is rare further north (JJD and JG, unpublished). A second larval parasitoid, later described as Tetrastichus planipennisi Yang (Fig. 9) (Yang et al., 2006), was found attacking EAB larvae from F. pennsylvanica and F. mandshurica trees planted in Jilin province (Liu et al., 2006). This gregarious larval endoparasitoid is also Figure 9 Adult Tetrastichus planipennisi. David Cappaert, found in Liaoning and Heilongjiang provinces (LSB and Michigan State University, Bugwood.org.

196 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

EAB or the following nontarget species (1) nine species of Agrilus, including three from the United States (A. anxius, A. bilineatus, and A. ruficollis [Fabricius]) and six from China (A. auriventris Saunders, A. inamoenus Kerremans, A. lewisiellus Kerremans, A. mali Matsumura, A. sorocinus Kurosawus, A. zanthoxylumi Li), (2) one other Chinese buprestid (), (3) one cerambycid from China ( gebleri Fann); (4) one curculionid from China (Eucryptorrhynchus chinensis); and (5) six lepidopterans from three families from China: Pyralidae (Ostrinia orientalis [Mutuura and Munroe], luteellus Motschulsky, Sylepta derogate F., unknown pyralid larvae), Cossidae (Holcocerus Figure 10 Adult Oobius agrili ovipositing in an emerald insularis Staudinger), and Carposinidae (Carposina niponensis ash borer egg. Debbie Miller, USDA Forest Service, Walsingham). Bugwood.org. Larvae of each species were implanted into their respective natural host plants before exposure to S. agrili sampled the previous fall at the same site in Jilin province adults. The results of these no-choice assays showed that (LSB, unpublished). S. agrili parasitized and developed only in the larvae of Russian Far East From 2009–2011, surveys for the following Agrilus species: A. anxius, A. bilineatus, A. EAB and its natural enemies in the Russian Far East led inamoenus, A. mali, and A. zanthoxylumi. Parasitism by S. to the recovery of three larval parasitoids: T. planipennisi, agrili was significantly lower in these nontarget species Atanycolus nigriventris Vojnovskaja-Krieger, and the than in EAB larvae (Yang et al., 2008). recently described Belokobylskij (Williams Using a Y-tube olfactometer, the behavioral responses et al., 2010; Belokobylskij et al., 2012). Among these, S. of adult S. agrili were assessed to leaf volatiles from 14 galinae is the dominant parasitoid of EAB in this part of woody plant species growing in China from the following Russia, parasitizing up to 63% of larvae collected from families: Oleaceae (2 spp.), Rutaceae (2 spp.), Rosaceae (3 F. pennsylvanica planted in and around Vladivostok (Duan spp.), Salicaceae (2 spp.), and one each in Celastraceae, et al., 2012a). In addition, an unidentified species of egg Juglandaceae, Leguminosae, and Simaroubaceae. Only the parasitoid (Hymenopteran: Encyrtidae) was collected leaves of F. velutina, F. pennsylvanica (Oleaceae), Prunus persica from EAB-infested ash trees (F. pennsylvanica) trees in L., and Ailanthus altissima (Mill.) Swingle were attractive Vladivostok (Duan et al., 2012c). to S. agrili females, supporting the view that EAB is its primary host in China (Yang et al., 2008). South Korea Spathius galinae, a species of Tetrastichus, The above cited authors also sampled other insects tentatively identified as Tetrastichus telon (Graham), and from F. velutina and other tree species at field sites in China, Teneroides maculicollis Lewis (Coleoptera: Cleridae) were recovering 17 species of wood-boring larvae, nine of found attacking EAB larvae in girdled ash trees in Daejeon which were buprestids and of those, six were Agrilus spp. in 2008 (Williams et al., 2010). Attempts to culture these (others were Cerambycidae and several were families of species in quarantine in the United States were unsuccessful. ). These wood-boring larvae were returned to the laboratory and reared for emergence of parasitoids, but Host Range Test Results neither S. agrili nor T. planipennisi emerged. However, other Spathius agrili The host specificity of S. agrili was hymenopteran parasitoid species reared from the larvae evaluated by comparing parasitism of EAB larvae to that of other species of Agrilus larvae included an unknown in other insect species using no-choice-laboratory assays Tetrastichus sp. from A. sorocinus in Tianjin; Tetrastichus performed in both the United States and China (Gould sp. and Doryctes sp. from A. mali, Tetrastichus sp. from A. et al., 2007; Yang et al., 2008). In these assays, groups of lewisiellus, Tetraichus sp., and an unknown braconid from A. female and male S. agrili were exposed to either larvae of zanthoxylumi from Shaanxi; Atanycolus sp. and Eupelmus sp.

XVII Emerald Ash Borer 197 The Use of Classical Biological Control to Preserve Forests in North America

from A. mali in Xinjiang; and Spathius sp. from A. auriventris [L.]) laid on ash branches. In the no-choice assays, O. agrili in Zhejiang (Yang et al., 2008). These findings support the did not parasitize eggs of the cerambycids, lepidopterans, host-specificity ofS. agrili in China. or those of the smaller Agrilus spp. (A. sucinctus, A. sulcicollis, A. egenus), although it did parasitize eggs of the Tetrastichus planipennisi The host specificity of larger Agrilus spp. (A. anxius, A. bilineatus, A. ruficollis). It T. planipennisi was evaluated by comparing EAB-larval was determined that Agrilus eggs laid by small Agrilus spp. parasitism to that of other insect species in the United States were about half the size of those Agrilus eggs accepted by using paired, no-choice laboratory assays with EAB larvae as O. agrili, suggesting that egg size may limit acceptance. positive controls (methods as per Badendreier, et al. [2005]). As a result, choice-laboratory assays were conducted by In these assays, groups of female and male T. planipennisi exposing O. agrili females to eggs of EAB and eggs from were exposed to larvae of EAB or other species that were each of the three larger Agrilus species on their respective similar in stage or size. Nontarget test species included eight hosts: A. anxius on birch (Betula), A. bilineatus on oak buprestids (A. anxius, A. bilineatus, A. ruficollis, A. subcinctus, (Quercus), and A. ruficollis on raspberry (Rubus). When given Lacordaire, (Olivier), C. a choice, O. agrili preferred the EAB eggs on ash vs. eggs floricola Gory, C. sexsignata Say), five cerambycids (Neoclytus of the other three species on their respective host plants. acuminatus F., Megacyllene robiniae Forster, Astylopsis sexguttata These results show that O. agrili prefers eggs of EAB on [Say], Monochamus scutellatus [Say], unknown sp. from apple), Fraxinus, but will parasitize eggs of larger Agrilus spp. and and one species of tenthredinid in the can physiologically develop inside them. (Janus abbreviates [Say]). The larvae of each species were implanted into their respective natural host plants. We Releases Made also assayed the following non-wood-boring insect larvae After research on O. agrili, T. planipennisi, and S. agrili by insertion into ash: Coleoptera: Tenebrionidae (Tenebrio biology, laboratory rearing, and host specificity was molitor L.), Lepidoptera: Pyralidae (Galleria mellonella L.), and completed in 2007, researchers submitted petitions to Lepidoptera: Sphinghidae (Manduca sexta L.). The latter the North American Plant Protection Organization was tested as a surrogate for sphinx (Sphingidae) (NAPPO) and permit requests to USDA , Plant that pollinate the eastern prairie fringed orchid (Platanthera Health Inspection Service (APHIS) for field release of leucophaea [Nuttall] Lindley), a federally listed threatened these parasitoid species for the biological control of EAB orchid found in Michigan. Larvae of M. sexta were also in the United States (NAPPO, 2012; USDA APHIS, exposed to T. planipennisi as they fed on tomato leaves 2012a). From the NAPPO petitions, APHIS compiled (Federal Register, 2007). Tetrastichus planipennisi rejected an Environmental Assessment, which was posted on the larvae of all species except EAB, indicating a narrow the Federal Register for public comment (Federal Register, host range for this species (Liu and Bauer, 2007; Federal 2007). Meanwhile, federal and state researchers and Register, 2007). regulatory agencies, university faculty, tribal councils, and Oobius agrili The host specificity of O. agrili was land managers evaluated the pros and cons of releasing evaluated by comparing O. agrili parasitism in EAB eggs these parasitoids in the United States for management laid on ash branches to those of other insect species in the of EAB. After the public comment period ended and a United States using both no-choice and choice assays with risk analysis was completed, APHIS posted a “finding EAB eggs as positive controls (Bauer and Liu, 2007; Federal of no significant impact” on the Federal Register (Federal Register, 2007). Female O. agrili females were exposed Register, 2007). Following final approval by Michigan, to eggs of EAB or those of six wood-boring buprestids APHIS issued release permits on July 23, 2007 to L. Bauer (A. anxius, A. bilineatus, A. egenus Gory, A. ruficollis, A. for release of O. agrili and T. planipennisi and to J. Gould for subcinctus, A. sulcicollis,) and two cerambycids (M. robiniae, release of S. agrili (Bauer et al., 2008). N. acuminatus) on their respective natural host trees. Also In the summer and fall of 2007, a combined total of tested were eggs of several lepidopteran species (Bombyx ~2,900 O. agrili, T. planipennisi, and S. agrili females (count mori L., Choristoneura rosaceana (Harris), M. sexta, Pieris rapae includes females only) were released at seven field sites in

198 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

Michigan (Bauer et al., 2008). The following year, similar numbers were released at 12 sites in Michigan, Ohio, and EVALUATION OF PROJECT OUTCOMES Indiana (Bauer et al., 2010). At this time, USDA APHIS determined there were no cost effective control methods Establishment of Agents and Effect on Pest to eradicate or prevent dispersal of EAB, and; therefore, EAB parasitoids are considered established in the field if they recommended that “authorities plan and prepare for they are detected by trapping or recovery from EAB eggs an infestation of EAB” (USDA APHIS, 2012b). According or larvae at least one year after a parasitoid species was last to principal researchers, demand for EAB parasitoids far released (Bauer et al., 2011; USDA FS AUSDA/F/NRS, exceeded supply, based on rearing in research laboratories. 2012). Depending on the species and the recovery method To increase supply, Forest Service and APHIS scientists and used, sampling for field recovery of EAB parasitoids is managers initiated the EAB Biological Control Program done in late summer or early fall when parasitoid densities (USDA APHIS, 2012c), which included the construction are highest, or during late winter or early spring after and staffing of the EAB Biocontrol Facility, an EAB parasitoids have broken diapause. The simplest parasitoid- parasitoid mass-rearing laboratory in Brighton, Michigan, recovery method involves felling EAB-infested ash trees, which became operational in 2009 after researchers placing logs in large cardboard-rearing tubes in a brightly successfully transferred rearing technology and parasitoid lit room, and collecting the parasitoid adults as they colonies (Bauer et al., 2010; Emeraldashborer, 2012). More emerge and enter clear collection cups attached to the than 34,000 female parasitoids (all species combined) ends of rearing tubes. This method works for emergence were produced in 2009, allowing for expanded releases in of the EAB parasitoids and other insects living in and on Michigan, Ohio, and Indiana, and the establishment of ash logs. Alternatively, the logs can be debarked and EAB new research sites in Maryland and Illinois. larvae and associated larval parasitoids collected from In 2010, USDA researchers wrote and posted the galleries. Parasitoids are then reared to the adult stage for online manual, Emerald Ash Borer Biological Control Release identification (Bauer et al., 2011). Guidelines, which provides information on EAB and Less-destructive sampling methods for recovery of parasitoid biology, data collection, release-site selection, O. agrili developing or diapausing inside EAB eggs (laid permits, and parasitoid-release methods. In 2012, the online on the outer bark of ash trees) include either collecting manual was updated and expanded to include methods for EAB eggs from the bark or placing egg-bearing bark determining parasitoid establishment or recovery from samples in cardboard rearing tubes for emergence of release sites and designated the “Emerald Ash Borer O. agrili adults. After the bark samples are dry, eggs are Biological Control Release and Recovery Guidelines” recovered from sifted debris and evaluated for parasitism (USDA FS APHIS/ARS/FS, 2012).During this time, by O. agrili. Alternatively, a trap to detect parasitoids can researchers continued to improve rearing methods and to be made by hanging logs, on which EAB eggs were laid transfer that technology to the EAB Biocontrol Facility, in the laboratory, on ash trees in the field. These “egg which led to improved parasitoid production (Ulyshen sentinel logs” are then retrieved from the field after ten et al., 2010; Gould et al., 2011a; Duan et al., 2011a). In to 14 days of exposure, and each egg is then examined for 2010, more than 100,000 female parasitoids (all species an O. agrili exit hole, dissected, or reared in the laboratory combined) were released in Michigan, Maryland, Illinois, to determine if the egg is parasitized (Bauer et al., 2013; Indiana West Virginia, Kentucky, and Minnesota. In 2011, USDA FS APHIS/ARS/FS, 2012). more than 200,000 parasitoids were reared and released in A similar, non-destructive method for recovery of the states already involved in EAB biological control research larval parasitoids uses small ash logs, in which last-instar and program releases, and new sites were started in New EAB larvae have been inserted under the bark. These “larval York, Pennsylvania, Virginia, and Wisconsin. To keep sentinel logs” are hung on ash trees in the field for a seven- track of parasitoid releases and recoveries, APHIS and FS day exposure period. The sentinel logs are then returned to collaborated with Michigan State University to develop an the laboratory, and each is examined for parasitoids or online database (Mapbiocontrol, 2012). reared for identification of adult parasitoids. Finally, yellow

XVII Emerald Ash Borer 199 The Use of Classical Biological Control to Preserve Forests in North America

pan traps can also be used to recover EAB parasitoid species the establishment of S. agrili remains unknown in more (Bauer et al., 2013; USDA FS APHIS/ARS/FS, 2012). southerly states, such as Maryland, West Virginia, and Since 2008, establishment of O. agrili, T. planipennisi, or Kentucky because releases were done relatively recently. S. agrili has been confirmed using a variety of methods at Until more information becomes available, APHIS plans many study sites in Michigan. More recently, one or more to continue to release this parasitoid in areas below 40 NL of the parasitoid species were recovered at release sites north (USDA–APHIS/ARS/FS, 2013). in Ohio, Maryland, Indiana, Illinois, and Pennsylvania (Bauer et al., 2009, 2010, 2011, 2013; Gould et al. 2011b). Nontarget Effects More detailed studies are ongoing at six long-term study Potential attack on nontarget Agrilus species. by the sites (each comprised of release and control plots) in introduced larval ectoparasitoid S. agrili was examined at southern Michigan, where O. agrili, T. planipennisi, and S. three sites in 2007, 2008, and 2009. Potted trees (large were released between 2007 and 2010. Since the last agrili nursery stock) of European paper birch (Betula pendula release of O. agrili at these long-term study sites in 2009, Roth) and pin oak (Quercus palustris Münch) were planted EAB-egg parasitism has been monitored annually, and at each site. To ensure these trees contained nontarget the establishment of O. agrili has been confirmed. From Agrilus larvae, adult bronze birch borers (A. anxius) were samples of EAB eggs and placement of egg sentinel logs caged on the birch trees and adults of the two-lined at sites, parasitism of EAB eggs was approximately 5% in chestnut borer (A. bilineatus) were caged on the oak trees. 2010 and 20% in 2011 (Duan et al., 2011b, 2012d; Abell Ash, birch, and oak trees were felled at each site during et al., 2011). In 2011, EAB-egg parasitism was found the following winter after sufficient chill to break insect from 73% of the sampled trees in parasitoid-release plots diapause. The logs were placed in cardboard-rearing tubes and 25% of trees in control plots, a dispersal of ~800 m in a warm environment to stimulate insect emergence. (LSB, unpublished). These results confirm that established All logs produced adult Agrilus, indicating that EAB and populations of O. agrili are expanding and gradually the nontarget hosts were available for attack by S. agrili. dispersing from the original release epicenters. The native S. floridanus was found attacking all three Changes in EAB larval parasitism are also being Agrilus species at all sites. In 2009, five S. agrili emerged monitored each year at these study sites by destructively from a birch log, showing parasitism of A. anxius, but no sampling EAB-infested ash trees (Duan et al., 2013). In parasitism by S. agrili from ash or oak logs was confirmed 2012, three to four years after T. planipennisi releases, the in 2008 or 2009. Although more S. agrili were released in proportion of sampled ash trees with at least one brood of 2010 and recovered from ash at all three sites, S. agrili was T. planipennisi increased steadily from 33% to 92% in the not reared from the test birch or oak logs that year. These parasitoid-release plots and from 4% to 83% in the control results support the results of laboratory host-range testing plots. Over the same period, EAB larval parasitism by T. that some parasitism of nontarget Agrilus species may planipennisi increased from 1.2% to 21.2% in the release occur in the field. plots and from 0.2% to 12.8% for the control plots. The results of this five-year study demonstrate thatT. planipennisi Recovery of Affected Tree Species or Ecosystems is established and spreading throughout EAB populations of southern Michigan (Duan et al., 2013, 2014). The population density of EAB is difficult to determine However, S. agrili has not been recovered from EAB in an absolute sense (number per unit area) and requires larvae sampled in southern Michigan one or two years after destructive sampling and considerable labor (McCullough release, although adults are occasionally recovered in yellow and Siegert, 2007b). Therefore, trends in EAB population pan traps (Bauer et al., 2011; Gould et al., 2011b). Gould et densities are based on indirect estimates using ash decline al. (in press) suggested poor recovery of S. agrili, which was and mortality over time (Smith, 2006). Parasitoids were originally collected in Tianjin, China (39th parallel north), introduced at seven EAB biological control research sites in resulted from incompatible climate matching Tianjin and Michigan and two sites in Ohio in 2008 and 2009. At each with northern regions of the United States. Although poor research site, a release plot was paired with a non-release synchrony with required host life stages may be a factor, control plot, and 50 ash trees >4-cm DBH were selected

200 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

and tagged in each plot. From 2008 to 2010, the following in supporting the survival of ash seedlings and saplings data were collected annually: GPS coordinates, crown class, that grow up in the aftermath of EAB. In the decades to epicormic shoots, EAB exit holes, DBH, and come, researchers will need to continue to monitor the feeding (Gould et al., 2011b). No significant differences relative importance of the various interactions affecting were found between ash health at the release and control ash survival and EAB population dynamics in North plots, with most of the larger trees dying from EAB attack America. before the exotic parasitoids were detectable at most sites. Future plans to assess the impact of EAB biological BIOLOGY AND ECOLOGY OF KEY control at these and other sites include documenting NATURAL ENEMIES growth and survival of young ash trees at the sites (the regrowth) and estimating the recruitment, growth, and Natural Enemies in the United States survival of these new trees as they become large enough In North America, eleven native to be susceptible to EAB attack. Antanyolus spp. species of Atanycolus are listed as parasitoids of Agrilus spp. (Marsh et al., 2009). These Atanycolus are solitary, Broad Assessment of Factors Affecting Success or ectoparasitic idiobionts of late-instar larvae, and several Failure of Project species parasitize EAB. Surveys of natural enemies in At a limited number of study sites in Michigan, where southeastern Michigan from 2003 to 2004 detected larval the EAB parasitoids from China were first introduced, parasitism of EAB by A. hicoriae and A. simplex; however, they are established and spreading, and their population total larval parasitism was <1% (Bauer et al., 2005). In densities are increasing. The long-term impact these 2007 and 2008, Cappaert and McCullough (2009) found parasitoids will have on ash health and recovery is not yet that EAB larval parasitism ranged from 9 to 71% by a known; however, the longevity and condition of North new species of Atanycolus, later described as A. cappaerti American ash species planted in northeast China and (Marsh et al., 2009). The following year, EAB populations the Russian Far East provide a basis for some optimism. collapsed in that area, and the prevalence of A. cappaerti Life-table studies in China and Russia indicate that the fell to <1% (Tluczek et al., 2010). In a different Michigan main mortality factors affecting EAB attacking North study, at sites where EAB populations were building, EAB American ash in Asia are egg and/or larval parasitoids. larval parasitism by Atanycolus spp. increased from <1% in To assess the effects of biological control in different 2009 to 19% in 2010 (Duan e al., 2012b). Of individuals ash species and genotypes across geographical regions, reared to the adult stage and identified (n=383) in that detailed data on ash density and health must be collected study, 93% were A. cappaerti, 5% were A. hicoriae, ~1% were over time and analyzed. A. tranquebaricae Shenefelt, and <1% were A. disputabilis. Biological control is a long-term but sustainable Atanycolus cappaerti is known to parasitize other species of management strategy, and EAB natural enemy complexes Agrilus in Michigan, indicating a broader host range for may eventually stabilize eventually and suppress host A. cappaerti than for other Atanycolus species (Cappaert population densities below a tolerance threshold allowing and McCullough 2009). Long-term studies are needed the survival and reproduction of native ash species. As to monitor successional changes occurring in parasitoid guilds associated with EAB populations, as EAB density the EAB invasion spreads across North America, most declines due to ash mortality and as the introduced ash trees die due the high EAB populations that develop parasitoids increase in density. in this abundant and susceptible resource. This tree mortality then results in collapse of EAB population, Oobius agrili This species is a solitary and partheno- and provides an intense selection event that may favor genic egg parasitoid discovered parasitizing EAB eggs the proliferation of EAB-resistant ash genotypes. In fact, sampled from ash trees in Jilin province, China, in 2004 several researchers are now screening the surviving ash (Zhang et al., 2005) and later in Liaoning province (JJD, trees in Michigan for EAB resistance. The parasitoids, unpublished) that has been released and established in both introduced and native species, are likely to be crucial the United States. Mature O. agrili larvae diapause during

XVII Emerald Ash Borer 201 The Use of Classical Biological Control to Preserve Forests in North America

the winter inside EAB eggs and typically complete two in Daejeon, South Korea (Baranchikov, 2008; Williams generations each year (Bauer and Liu, 2007). Adult et al., 2010; Duan al., 2012a). It was recently described as emergence is synchronized with the oviposition period of S. galinae, a new species (Belokobylskij et al., 2012). From EAB, starting in late June and continuing into September EAB natural enemy surveys of infested green ash trees (F. in China (Liu et al., 2007). Similar emergence phenology pennsylvanica) planted up to 40 years ago in Vladivostok, for O. agrili was detected in Michigan, with adults starting parasitism by S. galinae ranged from 27.5 to 75.5% (Duan to emerge in late June and peak parasitism in August (Abell al. 2012a). Spathius galinae overwinters as mature larvae or et al., 2011). When reared in the laboratory at 24ºC, O. agrili prepupae, and adults emerge from EAB galleries in early completes one generation every three days with a realized spring. In the Vladivostok region, S. galinae completes fecundity of ~80 female progeny (LSB unpublished). two to three generations each year producing six to 15 larvae per EAB larva (Belokobylskij et al., 2012; Duan et Phasgonophora sulcata Phasgonophora sulcata is a al. 2012a). It is being evaluated for possible release in the solitary endoparasitic koinobiont of larvae of native North United States for biological control of EAB, particularly in American Agrilus species (Barter, 1957, 1965; Côté and northern areas because of its greater cold-hardiness (Duan Allen, 1980). In eastern North America, P. sulcata also et al., 2012a). parasitizes EAB larvae (Bauer et al., 2004, 2005; Duan et al., 2012b). Adults of this large chalcidid can be readily Tetrastichus planipennisi This parasite, a gregarious observed ovipositing through the bark of EAB-infested endoparasitic koinobiont of EAB larvae, was discovered ash trees between June and August. Eggs and larvae of P. while surveying EAB-infested ash trees in Jilin and sulcata slowly develop in the hemocoel of EAB larvae, with Liaoning provinces in 2003 (Liu et al., 2003) and later in maturation and pupation occurring the next year, often as Heilongjiang province (Yang et al., 2006), and has been their host larva enters the prepupal stage (LSB and JJD, released and established in the United States. Tetrastichus unpublished). Laboratory studies are continuing on the planipennisi parasitizes all larval stages of EAB, overwinters biology of P. sulcata and to evaluate its impact on EAB as a larva, and completes up four generations each year populations in the field. in Jilin province (Liu et al., 2007). Adult emergence begins in April or May, and females begin parasitizing Spathius agrili A gregarious, ectoparasitic idiobiont overwintering A. planipennis larvae soon thereafter, with of late-instar EAB larvae, this parasitoid was first reported parasitism increasing up to 40% by August (Liu et al., in Tianjin province, China (Xu, 2003) and later in Jilin 2007). Similar emergence phenology was found for T. province (Liu et al., 2003; Yang et al., 2005) and has been planipennisi in Michigan, with adults starting to emerge in released and recovered in the United States. Spathius agrili late April or early May (LSB, unpublished). The results overwinter as mature larvae, and adults emerge in July and of a recent study suggest that T. planipennisi may be more August (Wang et al., 2006). In Michigan, adults began to effective at parasitizing EAB larvae in thin-barked, small emerge in mid-July and continued into mid-September diameter ash trees (<12-cm DBH) due to its relatively short (LSB, unpublished). When reared in the laboratory at a day: ovipositor (2.0 to 2.5 mm long) (Abell et al., 2012). When night temperature cycle of 25: 20ºC, has a 4:1 female: male reared in the laboratory at 25ºC, T. planipennisi completes sex ratio and an estimated realized fecundity of ~40 female one generation every 27 days, has a 4:1 female:male sex progeny during the female lifespan (average 61 days) (Wang ratio, and an average realized fecundity of ~45 female et al., 2008; Gould et al. 2011a). progeny during the female lifespan (average 42 days) (Liu Spathius galinae A gregarious, ectoparasitic and Bauer, 2007; Ulyshen et al., 2010; Duan et al., 2011a). idiobiont parasitoid, this species was recently discovered in Primorskiy Krai of the Russian Far East, but was initially identified as a similar, closely related species(Yurchenko et al., 2007). This species is being held (as of 2014) in USDA quarantine facility for study. This parasitoid was repeatedly collected from EAB larvae in and around Vladivostok and

202 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

Bauer, L. S., H-P. Liu, R. A. Haack, D. L. Miller, and T. R. REFERENCES Petrice. 2004. Natural enemies of emerald ash borer in southeastern Mchigan, pp. 33–34. In Mastro, V. and Abell, K. J., L. S. Bauer, D. L. Miller, J. J. Duan, and R. Van Driesche. 2011. Assessment of Oobius agrili phenology R. Reardon (comps.). Proceedings of the 2003 Emerald using egg stinel logs, pp. 99–100. In Mastro, V., D. Ash Borer Research and Technology Meeting, Port Huron, Lance, R. Reardon, and G. Parra (compilers). Proceedings Michigan. USDA Forest Service FHTET-2004-02. of the 2011 Emerald Ash Borer Research and Development http://www.fs.fed.us/foresthealth/technology/ Review Meeting, Wooster, Ohio. USDA Forest Service pdfs/2003EAB.pdf. FHTET-2011-06. http://www.fs.fed.us/foresthealth/ technology/pdfs/EAB_FHTET-2011-06.pdf. Bauer, L. S., H-P. Liu, R. A. Haack, R-T. Gao, T-H. Zhao, D. L. Miller, and T. R. Petrice. 2005. Update on emerald Abell, K. J., J. J. Duan, L. S. Bauer, J. P. Lelito, and R. G. Van Driesche. 2012. The effect of bark thickness on ash borer natural enemies in Michigan and China, the effectiveness of Tetrastichus planipennisi (Hymen: pp. 71–72. In Mastro, V. and R. Reardon (compilers). Eulophidae) and Atanycolus spp. (Hymen: Braconidae) Proceedings of the 2004 Emerald Ash Borer Research and two parasitoids of emerald ash borer (Coleop: Technology Meeting, Romulus, Michigan. USDA Forest Buprestidae). Biological Control 63: 320–325. Service FHTET-2004-15. http://www.nrs.fs.fed.us/ Akiyama, K. and S. Ohmomo. 1997. A Checklist of the Japanese pubs/9610 . Buprestidae. Gekkan-Mushi (Supplement 1). 67 pp. Bauer, L. S. and H-P. Liu. 2007. Oobius agrili (Hymentoptera: Alexeev, A. V. 1979. New, unknown till now on the territory Encyrtidae), a solitary egg parasitoid of emerald ash of USSR and hardly known species of buprestid- borer from China, pp. 63–64. In Mastro, V., D. Lance, beetles (Coleoptera, Buprestidae) from Eastern Siberia R. Reardon, and G. Parra (compilers). Proceedings of the and the Far East, pp.123–139. In Krivolutskaya, G. O. (ed.). Zhuki Dalnego Vostoka i Vostochnoi Sibiri (novye 2006 Emerald ash borer and Asian long-horned beetle Research dannye po faune i sistematike). Vladivostok, Russia. and Development Review Meeting, Cincinnati, Ohio. USDA Forest Service FHTET-2007-04. http://www.fs.fed.us/ Alexeev, A. V. 1998. To the subgeneric classification of the buprestid genus Agrilus Curtis (Coleoptera, foresthealth/technology/pdfs/EAB_ALB_2006.pdf. Buprestidae) of the Palaearctic Fauna. Entomological Bauer, L. S., H-P. Liu, D. L. Miller, and J. Gould. 2008. Review 78: 423–436. Developing a classical biological control program Anulewicz, A., D. G. McCullough, D. L. Cappaert, and T. for Agrilus planipennis (Coleoptera: Buprestidae), an M. Poland. 2008. Host range of the emerald ash borer invasive ash pest in North America. Newsletter of the ( Fairmaire) (Coleoptera: Buprestidae) Agrilus planipennis Michigan Entomological Society 53: 38–39. http://www. in North America: Results of multiple-choice field nrs.fs.fed.us/pubs/1439. experiments. Environmental Entomology 37: 230–241. Badendreier, D., F. Bilger, and U. Kuhlmann. 2005. Methods Bauer, L. S., H-P. Liu, and D. L. Miller. 2009. Emerald to assess nontarget effects of invertebrate biological ash borer biological control: rearing, releasing, control agents of pests. Biocontrol 50: 821– establishment, and efficacy of parsitoids, pp. 7–8. In 870. McManus, K. and K. Gottschalk (eds.). Proceedings of the Baranchikov, Y. N. 2008. Emerald ash borer has reached 20th USDA Interagency Research Forum on Europe, p. 7. In Gottschalk, K. (ed.). Proceedings of the 18th 2009, Annapolis, Maryland. USDA Forest Service NRS USDA Interagency Research Forum on Invasive Species 2007; General Technical Report NRS-P-51. http://nrs.fs.fed. Annapolis, MD. USDA Forest Service NRS General us/pubs/34230. Technical Report NRS-P-28. http://nrs.fs.fed.us/pubs/ gtr/gtr_nrs-p-28papers/03baranchikov-p-28.pdf. Bauer, L. S., J. Gould, H-P. Liu, M. Ulyshen, J-J. Duan, C. Sadof, A. Ziegler, and J. Lelito. 2010a. Update on Barter, G. W. 1957. Studies of the , Agrilus anxius Gory, in New Brunswick. The Canadian emerald ash borer biological control research in the U.S., Entomologist 89: 12–36. pp. 99–102. In Lance, D., R. Reardon, and V. Mastro Barter, G. W. 1965. Survival and development of the (compilers), Proceedings of the 2009 Emerald Ash Borer bronze poplar borer Agrilus liragus Barter & Brown Research and Technology Meeting, Pittsburgh, Pennsylvania. (Coleoptera: Buprestidae). The Canadian Entomologist USDA Forest Service FHTET-2010-01. http://www. 97: 1063–1068. fs.fed.us/foresthealth/technology/pdfs/2009EAB.pdf.

XVII Emerald Ash Borer 203 The Use of Classical Biological Control to Preserve Forests in North America

Bauer, L. S., J. Gould, J. Duan, and M. Ulyshen. 2011. Cappaert, D. and D. G. McCullough. 2009. Occurrence Emerald ash borer biological control, pp. 70–73. In and seasonal abundance of Atanycolus cappaerti McManus, K. and K. Gottschalk (eds.). Proceedings of the (Hymenoptera: Braconidae) a native parasitoid of 21nd USDA Interagency Research Forum on Invasive Species emerald ash borer, Agrilus planipennis (Coleoptera: 2010. Annapolis, Maryland. USDA Forest Service Buprestidae). The Great Lakes Entomologist 42: 16–29. General Technical Report NRS-P-75. http://nrs.fs.f/ Cappaert, D., D. G. McCullough, T. M. Poland, and N. W. YPT_Method.pdf. Siegert. 2005. Emerald ash borer in North America: a Bauer, L. S., J. Gould, J. Duan, J. Hansen, A. Cossé, D. Miller, research and regulatory challenge. American Entomologist K. Abell, R. Van Driesche, J. Lelito, and T. Poland. 2012. 51: 152–165. Sampling methods for recovery of exotic emerald ash borer parasitoids after environmental release, pp. 2–5. Chinese Academy of Science, Institute of Zoology. 1986. In McManus, K. and K. Gottschalk (eds.). Proceedings Agrilus marcopoli Obenberger, p. 445. In Editorial of the 22nd USDA Interagency Research Forum on Invasive committee (eds.). Agriculture Insects of China (Part I). Species 2011. Annapolis, Maryland. USDA Forest China Agriculture Press, Beijing, China. Service General Technical Report NRS-P-92. http:// Chamorro, M. L., M. G. Volkovitsh, T. M. Poland, R. A. nrs.fs.fed.us/pubs/39810. Haack, and S. W. Lingafelter. 2012. Preimaginal stages Bauer, L. S., J. J. Duan, K. Abell, J. Gould, J. Lelito, A. Storer, of the emerald ash borer, Agrilus planipennis Fairmaire and R. Van Driesche, Establishment of Oobius agrili, an (Coleoptera: Buprestidae): an invasive pest on ash trees introduced egg parasitoid of the emerald ash borer, in (Fraxinus). PLoS ONE 7: 1–12. http://www.nrs.fs.fed. the United States. In McManus, K. and K. Gottschalk us/pubs/jrnl/2012/nrs_2012_chamorro_001.pdf (eds.). Proceedings of the 24th USDA Interagency Research Chapman, R. N. 1915. Observations on the life history Forum on Invasive Species 2013. Annapolis, Maryland, of Agrilus bilineatus. Journal of Agricultural Research 3: USA. USDA Forest Service FHTET-2013-01. http:// 283–293. www.nrs.fs.fed.us/pubs/45421 Chittenden, F. H. 1897. The two-lined chestnut borer Bauer, L. S., J. Hansen, and J. Gould. 2013. Yellow pan traps: (Agrilus bilineatus Weber). USDA Entomological a simple method for trapping larval parasitoids released Division Circular No. 24, second series. 8 pp. for biological control of the emerald ash borer. http:// nrs.fs.fed.us/disturbance/invasive_species/eab/local- Côté, W. A., III and D. C. Allen. 1980. Biology of two- resources/downloads/YPT_Method.pdf lined chestnut borer, Agrilus bilineatus, in Pennsylvania and New York (Coleoptera: Buprestidae). Annals of the Bellamy, C. L. 2008. World catalogue and bibliography of Entomological Society of America 73: 409–413. the jewel beetles (Coleoptera: Bupretidae), pp. 1932– 2684. In Vol. 4. : Agrilina through Trachyini. Duan, J. J., R. W. Fuester, J. Wildonger, P. H. Taylor, S. Pensoft Series Faunistica No. 76, Pensoft Publishers, Sofia Barth, and S. E. Spichiger. 2009. Parasitoids attacking and Moscow. the emerald ash borer (Coleoptera: Buprestidae in western Pennsylvania. 92: 588–592. Belokobylskij, S. A., G. I. Yurchenko, A. Zaldívar-Riverón, Florida Entomologist J. Strazanac, and V. Mastro. 2012. A new emerald ash Duan, J. J., M. D. Ulyshen, L. S. Bauer, J. Gould, and R. Van borer (Coleoptera: Buprestidae) parasitoid species of Driesche. 2010. Measuring the impact of biotic factors Spathius Nees (Hymenoptera: Braconidae: ) on populations of immature emerald ash borers from the Russian Far East and South Korea. Annals of (Coleoptera: Buprestidae). Environmental Entomology 39: the Entomological Society of America 105: 165–178. 1513–1522. BenDor, T. K., S. S. Metcalf, L. E. Fontenot, B. Sangunett, Duan, J. J., C. B. Oppel, M. D. Ulyshen, L. S. Bauer, and and B. Hannon. 2006. Modeling the spread of the J. Lelito. 2011a. Biology and life history of Tetrastichus emerald ash borer. Ecological Modelling 197: 221–236. planipennisi (Hymenoptera: Eulophidae), a larval Bray, A. M., L. S. Bauer, T. M. Poland, R. A. Haack, A. endoparasitoid of the emerald ash borer. Florida I. Cognato, and J. J. Smith. 2011. Genetic analysis Entomologist 94: 933–940. of emerald ash borer (Agrilus planipennis Fairmaire) Duan, J. J., L. S. Bauer, M. D. Ulyshen, J. R. Gould, and populations in Asia and North America. Biological R. Van Driesche. 2011b. Development of methods Invasions 13: 2869–2887. for the field evaluation of Oobius agrili (Hymenoptera: Brown-Rytlewski, D. 2004. Tracking the emergence of Encurtidae) in North America, a newly introduced emerald ash borer adults. http://www.ipm.msu.edu/ egg parasitoid of emerald ash borer (Coleoptera: landreport/2004/EAB_tracking.pdf Buprestidae). Biological Control 56: 170–174.

204 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

Duan, J. J., G. Yurchenko, and R. Fuester. 2012a. Occurrence Federal Register. 2007. Availability of an environmental of emerald ash borer (Coleoptera: Buprestidae) and assessment for the proposed release of three biotic factors affecting its immature stages in far parasitoids for the biological control of the emerald eastern Russia. Environmental Entomology 41: 245–254. ash borer (Agrilus planipennis) in the continental United States. Federal Register 72: 28947–28948 [Docket No. Duan, J. J., L. S. Bauer, K. J. Abell, and R. Van Driesche. APHIS-2007-006]. http://www.regulations.gov/#!do 2012b. Population responses of hymenopteran cumentDetail;D=APHIS-2007-0060-0043. parasitoids to the emerald ash borer (Coleoptera: Fisher, W. S. 1928. A revision of the North American species Buprestidae) in recently invaded areas in north central of buprestid beetles belonging to the genus Agrilus. United States. BioControl 57: 199–209. United States National Museum Bulletin 145: 1–347. Duan, J. J., L. S. Bauer, J. Gould, and J. Lelito. 2012c. Fukutomi, K. and S. Hori. 2004. The buprestid beetles of Biological control of emerald ash borer: current Hokkaido in color (Coleoptera, Buprestidae). Jezoenss, progress and potential success. International Organization Sapporo 30: 1–25. of Biological Control Global Newsletter 34: 5. Gandhi, K. J. K. and D. A. Herms. 2010. Potential Duan, J. J., L. S. Bauer, J. A. Hansen, K. J. Abell, and R. loss due to impending devastation of the Van Driesche. 2012d. An improved method for North American genus Fraxinus by the exotic emerald monitoring parasitism and establishment of Oobius ash borer. Biological Invasions 12: 1839–1846. agrili (Hymenoptera: Encyrtidae), an egg parasitoid Gibson, G. A. P. 2005. The world species of Balcha Walker introduced for biological control of the emerald ash (Hymenoptera: Chalcidoidea: Eupelmidae), parasitoids borer (Coleoptera: Buprestidae) in North America. of wood-boring beetles. Zootaxa. EAB_ALB_2006.pdf Biological Control 60: 255–261. Gould, J. R., T. Ayer, and I. Fraser. 2011a. Effects of Duan, J. J., L. S. Bauer, K.J. Abell, J. P. Lelito, R. Van Driesche. rearing conditions on reproduction of Spathius agrili 2013. Establishment and abundance of Tetrastichus (Hymenoptera: Braconidae), a parasitoid of the planipennisi (Hymenoptera: Eulophidae) in Michigan: emerald ash borer (Coleoptera: Buprestidae). Journal of Potential for success in classical biocontrol of the Economic Entomology 104: 379–387. invasive emerald ash borer (Coleoptera: Buprestidae). Gould, J., L. Bauer, and J. Duan. 2011b. Update on recovery Journal of Economic Entomology 106:1145-1154. and establishment of parasitoids of the emerald ash Duan, J. J., K.J. Abell, L.S. Bauer, R. G. Van Driesche, 2014. borer. In Mastro, V., D. Lance, R. Reardon, and G. Parra (compilers). Proceedings of the 2011 Emerald Ash Natural enemies implicated in the regulations of an Borer Research and Development Review Meeting, Wooster, invasive pest: a life table analysis of the population Ohio. USDA Forest Service FHTET-2011-06. http:// dynamics of the invasive emerald ash borer. Agriculture www.fs.fed.us/foresthealth/technology/pdfs/EAB_ and Forest Entomology, (in press). FHTET-2011-06.pdf Dunbar, D. M. and G. R. Stephens. 1976. The bionomics of Gould, J. R., L. S. Bauer, J. J. Duan, K. J. Abell, and J. P. Lelito. the twolined chestnut borer, pp. 73–83. In Anderson, J. 2013 Emerald ash borer biological control: a decade of E. and H. K. Kaya (eds.). Perspectives in Forest Entomology. progress. In McManus, K. and K. Gottschalk (eds.). Connecticut Agricultural Experiment Station, New Proceedings of the 24th USDA Interagency Research Forum Haven, Connecticut, USA. on Invasive Species 2013, Annapolis, Maryland, USA. USDA Forest Service FHTET-2013-01. http://www. Emeraldashborer.info. 2012. Biological Control. http:// fs.fed.us/nrs/pubs/other/2013/2013_McManus_ emeraldashborer.info/biocontrol.cfm. FHTET-13-1.pdf EntSoc.org. Entomological Society of America. 2012. Grubov, V. I. 1982. Opredelitel sosudistych rastenij Common names of insects and related organisms. Mongolii.–Leningrad. (Engl. trans. 2001: Key to the http://www.entsoc.org/pubs/common_names Vascular Plants of Mongolia. Inc. Atlas. Vols. 1 and 2. Federal Register. 2003. Emerald ash borer: Quarantine and Science Publishers, Enfield.) Regulations. 7 CFR Part 301 [Docket No. 02-125-1]. Haack, R. A. and D. M. Benjamin. 1982. The biology and https://www.federalregister.gov/articles/2003/10/ ecology of the two-lined chestnut borer, Agrilus bilineatus 14/03-25881/emerald-ash-borer-quarantine-and- (Coleoptera: Buprestidae), on oaks, Quercus spp., in regulations Wisconsin. The Canadian Entomologist 114: 385–396.

XVII Emerald Ash Borer 205 The Use of Classical Biological Control to Preserve Forests in North America

Haack, R. A., E. Jendek, H-P. Liu, K. Marchant, T. Petrice, Liu, H-P. and L. S. Bauer. 2007. Tetrastichus planipennisi T. Poland, and H. Ye. 2002. The emerald ash borer: (Hymenoptera: Eulophidae), a gregarious larval a new exotic pest in North America. Newsletter of the endoparasitoid of emerald ash borer from China, Michigan Entomological Society 47:1–5. http://nrs.fs.fed. pp. 61–62. In Mastro, V., D. Lance, R. Reardon, and us/pubs/jrnl/2002/nc_2002_Haack_001.pdf G. Parra (compilers). 2006. Emerald ash borer and Asian long-horned beetle. Research and Development Review Hou, T-Q. 1993. Agrilus marcopoli Obenberger, p. 237. In Meeting, Cincinnati, Ohio. USDA FS FHTET 2007- Editorial committee (eds.) Fauna of Shandong Forest 04. http://nrs.fs.fed.us/pubs/9566 Insects. China Forestry publishing House. Beijing, Liu, H-Q., R-S. Ma, and Q-H. Li. 1996. Survey and manage- China. ment of emerald ash borer, Agrilus marcopoli. Agri- Izhevskii S. S. and E. G. Mozolevskaya. 2010. Agrilus Forestry Science and Technology of Tianjin 1: 46–48. planipennis Fairmaire in Moscow ash trees. Russian Liu, H-P., L. S. Bauer, R-T. Gao, T. H. Zhao, T. R. Petrice, Journal of Biological Invasions 1: 153–155. and R. A. Haack. 2003. Exploratory survey for the Jendek, E. 1994. Studies in the East Palaearctic species of emerald ash borer, Agrilus planipennis (Coleoptera: the genus Agrilus Dahl, 1823 (Coleoptera: Buprestidae). Buprestidae), and its natural enemies in China. The Great Lakes Entomologist 36: 191–204. http://nrs.fs.fed. Part I. Entomological Problems 25: 9–24. us/pubs/jrnl/2003/nc_2003_liu_001.pdf Jendek, E. and V. V. Grebennikov. 2011. Agrilus (Coleoptera, Liu, H-P., L. S. Bauer, D. L. Miller, T-H. Zhao, R-T. Buprestidae) of East Asia. Jan Farkac, Prague. 362 pp. Gao, L. Song, Q. Luan, R. Jin, and C. Gao. 2007. Kashian, D. M. and J. A. Witter. 2011. Assessing the Seasonal abundance of Agrilus planipennis (Coleoptera: potential for ash canopy tree replacement via current Buprestidae) and its natural enemies Oobius agrili regeneration following emerald ash borer-caused (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi mortality on southeastern Michigan landscapes. Forest (Hymenoptera: Eulophidae) in China. Biological Control Ecology and Management 261: 480–488. 42: 61–71. Loerch, C. R. and E. A. Cameron. 1983. Natural enemies Ko, J-H. 1969. A List of Forest Insect Pests in Korea. Forest of immature stages of the bronze birch borer, Agrilus Research Institute, Seoul, Korea. 458 pp. anxius (Coleoptera: Buprestidae), in Pennsylvania. Kovacs, K. F., R. G. Haight, D. G. McCullough, R. J. Mercader, Environmental Entomology 12: 1798–1801. N. W. Siegert, and A. M. Liebhold. 2010. Cost of MacFarlane, D. W. and S. P. Meyer. 2005. Characteristics potential emerald ash borer damage in U.S communities, and distribution of potential ash tree hosts for emerald 2009–2019. Ecological Economics 69: 569–578. ash borer. Forest Ecology and Management 213: 15–24. Kula, R. R., K. S. Knight, J. Rebbeck, D. L. Cappaert, L. MapBioControl. 2012. Agent release tracking and data S. Bauer, and K. J. K. Gandhi. 2010. Leluthia astigma management for federal, state, and researchers releasing (Ashmead) (Hymenoptera: Braconidae: Doryctinae) as three biocontrol agents released against emerald ash a parasitoid of Agrilus planipennis Fairmaire (Coleoptera: borer. http://www.mapbiocontrol.org/ Buprestidae: Agrilinae), with an assessment of host Marsh, P. M., J. S. Strazanac, and S. Y. Laurusonis. associations for Nearctic species of Leluthia Cameron. 2009. Description of a new species of Atanycolus Proceedings of the Entomological Society of Washington 112: (Hymenoptera: Braconidae) from Michigan reared 246–257. from the emerald ash borer. Great Lakes Entomologist 42: 8–15. Kurosawa, Y. 1956. Buprestid fauna of Eastern Asia (3). Bulletin of the National Science Museum (Tokyo) 3: 33–41. McCullough, D. G. and N. W. Siegert. 2007a. Using girdled trap trees effectively for emerald ash borer detection, Kurosawa, Y., S. Hisamatsu, and H. Sasaji (eds.). 1985. The delimitation, and survey. http://www.emeraldashborer. Coleoptera of Japan in Color Vol. 3. Hoikusha Publishing, info/files/handoutforpdf.pdf Osaka, Japan. McCullough, D. G. and N. W. Siegert. 2007b. Estimating Liu, Y-G. 1966. A study on the ash buprestid beetle, Agrilus potential emerald ash borer (Agrilus planipennis sp. in Shenyang. Annual Report of Shenyang Horticulture Fairmaire) populations using ash inventory data. Journal Research Institute, Shenyang, Liaoning, China. 16 pp. of Economic Entomology 100: 1577–1586.

206 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

McCullough, D. G., T. M. Poland, and D. Cappaert. 2009a. Poland, T. M. and D. G. McCullough. 2006. Emerald ash Attraction of the emerald ash borer to ash trees borer: invasion of the and the threat to stressed by girdling, herbicide, or wounding. Canadian North America’s ash resource. Journal of Forestry April- Journal of Forest Research 39: 1331–1345. May: 118–124. McCullough, D. G., T. M. Poland, A. C. Anulewicz, and Poole, R. W. 1997. Nomina insecta Nearctica: a check list D. Cappaert. 2009b. Emerald ash borer (Coleoptera: of insects of North America. Nomina series 1: 64–66. Buprestidae) attraction to stressed or baited ash trees. Pugh, S. A., A. M. Liebhold, and R. S. Morin. 2011. Changes Environmental Entomology 38: 1668–1679. in ash tree demography associated with the emerald ash borer invasion, indicated by regional forest inventory Mercader, R. J., N. W. Siegert, A. M. Liebhold, and D. G. data from the Great Lakes States. Canadian Journal of McCullough. 2011. Influence of foraging behavior and Forest Research 41: 2165–2175. host spatial distribution on the localized spread of the emerald ash borer, Agrilus planipennis. Population Ecology Rebek, E. J., D. A. Herms, and D. R. Smitley. 2008. 53: 271–285. Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North Muirhead, J. R., B. Leung, C. van Overdijk, D. W. Kelly, K. American and Asian ash (Fraxinus spp.). Environmental Nandakumar, K. R. Marchant, and H. J. MacIsaac. 2006. Entomology 37: 242–246. Modelling local and long-distance dispersal of invasive Schaefer, P. W. 2004. Agrilus planipennis (=A. marcopoli) emerald ash borer Agrilus planipennis (Coleoptera) in (Coleoptera: Buprestidae) in Japan and Mongolia: North America. Diversity and Distributions 12: 71–79. preliminary findings, p. 13. In Mastro, V. and R. Reardon Mühle, H. 2003. Taiwanese buprestids (Coleoptera, (compilers). Proceedings of the 2003 Emerald Ash Borer Buprestidae). Journal of the Zoology Society Wallacea 1: Research and Technology Meeting, Port Huron, Michigan. 43–48. USDA FS FHTET-2004-2. http://www.fs.fed.us/ foresthealth/technology/pdfs/2003EAB.pdf NAPPO (North American Plant Protection Organization). 2012. Guidelines for petition for first release of non- Schaefer, P. W. 2005. Foreign exploration for emerald ash indigenous entomophagous biological control agents. borer and its natural enemies, pp. 67–68. In Mastro, http://www.nappo.org/en/data/files/download/ V. and R. Reardon (compilers). Proceedings of the 2004 Emerald Ash Borer Research and Technology Meeting, PDF/RSPM12-Rev20-10-08-e.pdf Romulus, Michigan. USDA FS FHTET-2004-15. Nash, R. W., E. J. Duda, and N. H. Gray. 1951. Studies on http://www.fs.fed.us/foresthealth/technology/ extensive dying, regeneration, and management of pdfs/2004EAB.pdf birch. Maine Forest Service Bulletin 15. 82 pp. Siegert, N. W., D. G. McCullough., A. M. Liebhold, Nowak, D., D. Stevens, J. Crane, and J. Walton. 2003. and F. W. Telewski. 2009. Reconstruction of the Potential damage from emerald ash borer. http:// establishment and spread of the emerald ash borer: nrs.fs.fed.us/disturbance/invasive_species/eab/local- dendrochronological analysis, p. 70 In McManus, K. resources/downloads/EAB_potential.pdf and K. Gottschalk (eds.). 19th Annual Proceedings of the USDA Interagency Research Forum on Invasive Species. Parsons, G. 2008. Emerald ash borer, Agrilus planipennis General Technical Report NRS-P-36. http://www.nrs. Fairmaire (Coleoptera: Buprestidae), a guide to fs.fed.us/pubs/gtr/gtr_nrs-p-36.pdf identification and comparison to similar species. 56 Smith, A. 2006. Effects of community structure on forest pp. http://www.emeraldashborer.info/files/eab_id_ susceptibility and response to the emerald ash borer guide.pdf invasion of the Huron River watershed in southeast Petrice, T. R., R. A. Haack, and J. P. Lelito. 2009. Biology Michigan. M.S. Thesis, The Ohio State University. and larval morphology of Agrilus subcinctus (Coleoptera: Solomon, J. D. 1995. Guide to Insect Borers in North American Buprestidae), with comparisons to the emerald ash Broadleaf Trees and Shrubs. Agriculture Handbook No. borer, Agrilus planipennis. The Great Lakes Entomologist 706, USDA Forest Service, Washington, D. C. 735 pp. 53: 173–184. Tang, Y-L., X-Y. Wang, Z-Q. Yang, J. Jiang, X-H. Wang, Prasad, A. M., L. R. Iverson, M. P. Peters, J. M. Bossenbroek, and J. Lu. 2012. Alternative hosts of Sclerodermus and S. N. Matthews. 2010. Modeling the invasive pupariae (Hymenoptera: Bethylidae), a larval parasitoid emerald ash borer risk of spread using a spatially of the Massicus raddei (Coleoptera: explicit cellular model. Landscape Ecology 25: 353–369. Cerambycidae). Acta Entomologca Sinica 55: 55–62.

XVII Emerald Ash Borer 207 The Use of Classical Biological Control to Preserve Forests in North America

Taylor, P., J. J. Duan, R. W. Fuester, M. Hoddle, and R. Vansteenkiste, D.V., L. Tirry, J. Van Acker, and M. Stevens. Van Driesche. 2012. Parasitoid guilds of Agrilus 2005. Predispositions and symptoms of Agrilus borer woodborers (Coleoptera: Buprestidae): their diversity attack in declining oaks. Annals of Forest Science 61: and potential for use in biological control. Psyche 815–823. 813929: 1–10. http://www.hindawi.com/journals/ psyche/2012/813929/ Volkovitsh, M. G. and T. J. Hawkeswood. 1990. The larvae Taylor, R. A. J., L. S. Bauer, T. P. Poland, and K. Windell. of Agrilus australasiae Laporte and Gory and Ethon affine 2010. Flight performance of Agrilus planipennis Laporte and Gory. Spixiana 13: 43–59. (Coleoptera: Buprestidae) on a flight mill and in free Wang, X-Y., Z-Q, Yang, G-J. Liu, and E-S. Liu. 2006. flight.Journal of Insect Behavior 23: 128–148. Relationships between the emergence and oviposition Tluczek, A. R., D. Cappaert, and D. G. McCullough. 2010. of ectoparasitoid Spathius agrili Yang and its host Life cycle of Atanycolus sp. nr. hicoriae, a newly described emerald ash borer, Agrilus planipennis Fairmaire. Acta native parasitoid of emerald ash borer, pp. 91–92. In Ecologica Sinica 26: 1103–1109 Lance, D., R. Reardon, and V. Mastro (compilers). Proceedings of the 2009 Emerald Ash Borer Research and Wang, X., Z. Yang, H. Wu, and J. Gould. 2008. Effects of Technology Meeting, Pittsburgh, Pennsylvania. USDA FS host size on the sex ratio, clutch size, and size of adult FHTET-2010-1. http://www.fs.fed.us/foresthealth/ Spathius agrili, an ectoparasitoid of emerald ash borer. technology/pdfs/2009EAB.pdf Biological Control 44: 7–12. Tluczek, A. R., D. G. McCullough, and T. M. Poland. Wang, X-Y., Z-Q. Yang, J. R. Gould, Y-N. Zhang, G-J. Liu, 2011. Influence of host stress on emerald ash borer and E-S. Liu. 2010. The biology and ecology of the (Coleoptera: Buprestidae) adult density, development, emerald ash borer, , in China and distribution in trees. Agrilus planipennis . Journal Environmental Entomology 40: 357–366. of Insect Science 10: 1–22. Ulyshen, M. D., J. J. Duan, and L. S. Bauer. 2010. Suitability Wei, X., R. Reardon, Y. Wu and J-H. Sun. 2004. Emerald and accessibility of immature Agrilus planipennis ash borer, Agrilus planipennis Fairmaire (Coleoptera: (Coleoptera: Buprestidae) stages to Tetrastichus Buprestidae), in China: a review and distribution planipennisi (Hymenoptera: Eulophidae). Journal of survey. Acta Entomologica Sinica 47: 679–685. Economic Entomology 103: 1080–1085. Wessels-Berk B. and E-J. Scholte. 2008. One beetle too USDA FS APHIS/ARS/FS (Animal Plant Health Inspection many: the emerald ash-borer, Agrilus planipennis Service/Agricultural Research Service/Forest Service). (Coleoptera: Buprestidae), threatens trees in 2013. Emerald Ash Borer Biological Control Release Fraxinus and Recovery Guidelines. USDA APHIS-FS-ARS, Europe. Proceedings of the Netherlands Entomological Society Riverdale, Maryland. http://www.aphis.usda.gov/ Meeting 19: 165–168. plant_health/plant_pest_info/emerald_ash_b/ Williams, D., H-P. Lee, and Y-S. Jo. 2005. Exploration for downloads/EAB-FieldReleasGuidelines.pdf natural enemies of emerald ash borer in South Korea USDA APHIS. 2012a. Permits. PPQ 526. http://www. during 2004, p. 66. In Mastro, V. and R. Reardon. aphis.usda.gov/permits/login_epermits.shtml (compilers). Proceedings of the 2004 Emerald Ash Borer USDA APHIS. 2012b. Emerald ash borer program Research and Technology Meeting, Romulus, Michigan. manual, ver. 1.2, revised 2011. http://www.aphis. USDA FS FHTET-2004-15. http://www.fs.fed.us/ usda.gov/import_export/plants/manuals/domestic/ foresthealth/technology/pdfs/2004EAB.pdf. downloads/emerald_ash_borer_manual.pdf Williams, D., H-P. Lee, and Y-S. Jo. 2006. Exploration for USDA APHIS. 2012c. Emerald ash borer biological control program: 5-Year implementation strategy (FY10- emerald ash borer and its natural enemies in South FY14). http://www.aphis.usda.gov/plant_health/ Korea during May–June 2005, p. 52. In Mastro, and plant_pest_info/emerald_ash_b/downloads/eab- V., R. Reardon (compilers). Proceedings of the 2005 biocontrol-5yr-plan.pdf Emerald Ash Borer Research and Technology Meeting, USDA APHIS. 2012d. Initial county EAB detection map, Pittsburgh, Pennsylvania. USDA FS FHTET-2005-16. June 1, 2012. http://www.aphis.usda.gov/plant_ http://www.fs.fed.us/foresthealth/technology/ health/plant_pest_info/emerald_ash_b/ pdfs/2005EAB.pdf

208 Emerald Ash Borer XVII The Use of Classical Biological Control to Preserve Forests in North America

Williams, D., H-P. Lee, Y-S. Jo, G. I. Yurchenko, and V. C. Yang, Z-Q., Y-X. Yao, and X-Y. Wang. 2006. A new species Mastro. 2010. Exploration for emerald ash borer and of emerald ash borer parasitoid from China belonging its natural enemies in South Korea and the Russian to the genus Tetrastichus (Hymenoptera: Eulophidae). Far East 2004-2009, pp. 94–95. In Lance, D., R. Proceedings of the Entomological Society of Washington 108: Reardon, and V. Mastro (compilers). Proceedings of the 550–558. 2009 Emerald Ash Borer Research and Technology Meeting, Yu, C-M. 1992. Agrilus marcopoli Obnberger, pp. 400– Pittsburgh, Pennsylvania. USDA FS FHTET-2010-1. 401. In Xiao, G-R. (ed.). Forest Insects of China (2nd http://www.fs.fed.us/foresthealth/technology/ edition). China Forestry Publishing House, Beijing, pdfs/2009EAB.pdf China. (in Chinese) Translation: http://nrs.fs.fed.us/ Wu, H., X-Y. Wang, M-L. Li, Z-Q. Yang, F-X. Zeng, disturbance/invasive_species/eab/local-resources/ H-Y. Wang, L. Bai, S-J. Liu, and J. Sun. 2008. Biology downloads/biologyYu1992.pdf and mass rearing of Sclerodermus pupariae Yang et Yurchenko, G. I., G. I. Turova, and E. A. Kuzmin. 2007. Yao (Hymenoptera: Bethylidae), an important The distribution and ecology of emerald ash borer ectoparasitoid of the emerald ash borer, Agrilus (Agrilus planipennis Fairmare) in the Russian Far East, planipennis (Coleoptera: Buprestidae) in China. Acta pp. 94–98. In Kuretsov, A. I. Annual Memorial Meetings. Entomologica Sinica 51: 46–54. Issue XYIII. Vladivostok: Dalnauka, 2007. (ISBN Xu, G-T. 2003. Agrilus marcopoli Obnberger, pp. 321–322. 978-5-8044-0860-6). In Xu, G-T. (ed.). Atlas of Ornamental Pests and Diseases. Zhang, L-Y, Z-X. Chen, G-D. Yang, Q-Y. Huang, and Q-S. China Agriculture Press, Beijing, China. Huang. 1995. Control techniques of Agrilus marcopoli Yang, Z-Q., C. V. Achterberg, W-Y. Choi, and P. M. Marsh. on velvet ash, Fraxinus velutina. Bulletin of Horticulture 2005. First recorded parasitoid from China of Agrilus Science and Technology of Tianjin 26: 1–7. planipennis: a new species of Spathius (Hymenoptera: Zhang, Y-Z, D-W. Huang, T-H. Zhao, H-P. Liu, and L. Braconidae: Doryctinae). Annals of the Entomological S. Bauer. 2005. Two new species of egg parasitoids 98: 636–642. Society of America (Hymenoptera: Encyrtidae) of wood-boring beetle Yang, Z-Q., X-Y. Wang, J. R. Gould, and H. Wu. 2008. pests from China. Phytoparasitica 53: 253–260. Host specificity of Yang (Hymenoptera: Spathius agrili Zhao, T-H., R-T. Gao, H-P. Liu, L. S. Bauer, and L-Q. Braconidae), an important parasitoid of the emerald Sun. 2005. Host range of emerald ash borer, ash borer. Biological Control 47: 216–221. Agrilus planipennis Fairmaire, its damage and the Yang, Z-Q., X-Y. Wang, Y-X. Yao, J. R. Gould, and L-M. countermeasures. Acta Entomologica Sinica 48: 594–59. Cao. 2012. A new species of Sclerodermus (Hymenoptera: Bethylidae) parasitizing Agrilus planipennis (Coleoptera: Buprestidae) from China, with a key to Chinese species in the genus. Annals of the Entomological Society of America 105: 619–627.

XVII Emerald Ash Borer 209 The Use of Classical Biological Control to Preserve Forests in North America

Editors

Roy Van Driesche Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts

Richard Reardon Forest Health Technology Enterprise Team USDA, Forest Service, Morgantown, West Virginia

USDA Forest Service Publication FHTET–2013–2 September 2014